A Realistic Mixture of Persistent Organic Pollutants Affects Zebrafish Development, Behavior, and Specifically Eye Formation by Inhibiting the Condensin I Complex
Chemical Health and Safety; Health, Toxicology and Mutagenesis; Toxicology; SVHC; persistent organic pollutants; PFOS; zebrafish development; behaviour; condesin I
Abstract :
[en] Persistent organic pollutants (POPs) are posing major environmental and health threats due to their stability, ubiquity, and bioaccumulation. Most of the numerous studies of these compounds deal with single chemicals, although real exposures always consist of mixtures. Thus, using different tests, we screened the effects on zebrafish larvae caused by exposure to an environmentally relevant POP mixture. Our mixture consisted of 29 chemicals as found in the blood of a Scandinavian human population. Larvae exposed to this POP mix at realistic concentrations, or sub-mixtures thereof, presented growth retardation, edemas, retarded swim bladder inflation, hyperactive swimming behavior, and other striking malformations such as microphthalmia. The most deleterious compounds in the mixture belong to the per- and polyfluorinated acids class, although chlorinated and brominated compounds modulated the effects. Analyzing the changes in transcriptome caused by POP exposure, we observed an increase of insulin signaling and identified genes involved in brain and eye development, leading us to propose that the impaired function of the condensin I complex caused the observed eye defect. Our findings contribute to the understanding of POP mixtures, their consequences, and potential threats to human and animal populations, indicating that more mechanistic, monitoring, and long-term studies are imperative.
Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie
Language :
English
Title :
A Realistic Mixture of Persistent Organic Pollutants Affects Zebrafish Development, Behavior, and Specifically Eye Formation by Inhibiting the Condensin I Complex
H2020 - 722634 - PROTECTED - PROTECTion against Endocrine Disruptors; Detection, mixtures, health effects, risk assessment and communication.
Name of the research project :
PROTECTion against Endocrine Disruptors
Funders :
EU - European Union
Funding number :
722634
Funding text :
This project has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie Innovative Training Network (ITN) program PROTECTED, Grant agreement No. 722634.
United Nations Stockholm Convention on Persistent Organic Pollutants Treaty Ser. 2006 2256 119
European Parliament and Council Regulation (EC) No 850/2004 of the European Parliament and of the Council of 29 April 2004 on persistent organic pollutants and amending Directive 79/117/EEC Off. J. Eur. Union 29 April 2004 L158/157–149
Guo W. Pan B. Sakkiah S. Yavas G. Ge W. Zou W. Tong W. Hong H. Persistent Organic Pollutants in Food: Contamination Sources, Health Effects and Detection Methods Int. J. Environ. Res. Public Health 2019 16 4361 10.3390/ijerph16224361
Gregoraszczuk E.L. Ptak A. Endocrine-Disrupting Chemicals: Some Actions of POPs on Female Reproduction Int. J. Endocrinol. 2013 2013 828532 10.1155/2013/828532 23762054
Brody J.G. Moysich K.B. Humblet O. Attfield K.R. Beehler G.P. Rudel R.A. Environmental pollutants and breast cancer: Epidemiologic studies Cancer 2007 109 2667 2711 10.1002/cncr.22655
Sanderson J.T. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals Toxicol. Sci. 2006 94 3 21 10.1093/toxsci/kfl051 16807284
Ljunggren S.A. Helmfrid I. Salihovic S. van Bavel B. Wingren G. Lindahl M. Karlsson H. Persistent organic pollutants distribution in lipoprotein fractions in relation to cardiovascular disease and cancer Environ. Int. 2014 65 93 99 10.1016/j.envint.2013.12.017
Van Oostdam J.C. Dewailly E. Gilman A. Hansen J.C. Odland J.O. Chashchin V. Berner J. Butler-Walker J. Lagerkvist B.J. Olafsdottir K. et al. Circumpolar maternal blood contaminant survey, 1994–1997 organochlorine compounds Sci. Total Environ. 2004 330 55 70 10.1016/j.scitotenv.2004.02.028
Knutsen H.K. Kvalem H.E. Thomsen C. Froshaug M. Haugen M. Becher G. Alexander J. Meltzer H.M. Dietary exposure to brominated flame retardants correlates with male blood levels in a selected group of Norwegians with a wide range of seafood consumption Mol. Nutr. Food Res. 2008 52 217 227 10.1002/mnfr.200700096
Polder A. Skaare J.U. Skjerve E. Loken K.B. Eggesbo M. Levels of chlorinated pesticides and polychlorinated biphenyls in Norwegian breast milk (2002–2006), and factors that may predict the level of contamination Sci. Total Environ. 2009 407 4584 4590 10.1016/j.scitotenv.2009.04.032
Haug L.S. Salihovic S. Jogsten I.E. Thomsen C. van Bavel B. Lindstrom G. Becher G. Levels in food and beverages and daily intake of perfluorinated compounds in Norway Chemosphere 2010 80 1137 1143 10.1016/j.chemosphere.2010.06.023 20599247
Berntsen H.F. Berg V. Thomsen C. Ropstad E. Zimmer K.E. The design of an environmentally relevant mixture of persistent organic pollutants for use in in vivo and in vitro studies J. Toxicol. Environ. Health Part A 2017 80 1002 1016 10.1080/15287394.2017.1354439 28854125
McComb J. Mills I.G. Muller M. Berntsen H.F. Zimmer K.E. Ropstad E. Verhaegen S. Connolly L. Human blood-based exposure levels of persistent organic pollutant (POP) mixtures antagonise androgen receptor transactivation and translocation Environ. Int. 2019 132 105083 10.1016/j.envint.2019.105083 31470217
Doan T.Q. Berntsen H.F. Verhaegen S. Ropstad E. Connolly L. Igout A. Muller M. Scippo M.L. A mixture of persistent organic pollutants relevant for human exposure inhibits the transactivation activity of the aryl hydrocarbon receptor in vitro Environ. Pollut. 2019 254 113098 10.1016/j.envpol.2019.113098 31479813
Yadav A. Amber M. Zosen D. Labba N.A. Huiberts E.H.W. Samulin Erdem J. Haugen F. Berntsen H.F. Zienolddiny S. Paulsen R.E. et al. A human relevant mixture of persistent organic pollutants (POPs) and perfluorooctane sulfonic acid (PFOS) enhance nerve growth factor (NGF)-induced neurite outgrowth in PC12 cells Toxicol. Lett. 2021 338 85 96 10.1016/j.toxlet.2020.12.007
Amber M. Xie Y. Berntsen H.F. Zimmer K.E. Ropstad E. Verhaegen S. Connolly L. Effects of Defined Mixtures of Persistent Organic Pollutants (POPs) on Pre-lethal Cytotoxicity in the Human A-498 Kidney Cell Line In Vitro Expo. Health 2021 13 465 475 10.1007/s12403-021-00396-7
Segner H. Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption Comp. Biochem. Physiol. C Toxicol. Pharm. 2009 149 187 195 10.1016/j.cbpc.2008.10.099
Herkenne S. Ek O. Zamberlan M. Pellattiero A. Chergova M. Chivite I. Novotna E. Rigoni G. Fonseca T.B. Samardzic D. et al. Developmental and Tumor Angiogenesis Requires the Mitochondria-Shaping Protein Opa1 Cell Metab. 2020 31 987 1003.e1008 10.1016/j.cmet.2020.04.007
Lammer E. Carr G.J. Wendler K. Rawlings J.M. Belanger S.E. Braunbeck T. Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test? Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2009 149 196 209 10.1016/j.cbpc.2008.11.006
Westerfield M. A guide for the laboratory use of zebrafish (Danio rerio) The Zebrafish Book 5th ed. University of Oregon Press Eugene, OR, USA 2007
Pruvot B. Quiroz Y. Voncken A. Jeanray N. Piot A. Martial J.A. Muller M. A panel of biological tests reveals developmental effects of pharmaceutical pollutants on late stage zebrafish embryos Reprod. Toxicol. 2012 34 568 583 10.1016/j.reprotox.2012.07.010
Philip A.M. Wang Y. Mauro A. El-Rass S. Marshall J.C. Lee W.L. Slutsky A.S. dosSantos C.C. Wen X.Y. Development of a zebrafish sepsis model for high-throughput drug discovery Mol. Med. 2017 23 134 148 10.2119/molmed.2016.00188 28598490
Dalcq J. Pasque V. Ghaye A. Larbuisson A. Motte P. Martial J.A. Muller M. Runx3, Egr1 and Sox9b form a regulatory cascade required to modulate BMP-signaling during cranial cartilage development in zebrafish PLoS ONE 2012 7 e50140 10.1371/journal.pone.0050140
Larbuisson A. Dalcq J. Martial J.A. Muller M. Fgf receptors Fgfr1a and Fgfr2 control the function of pharyngeal endoderm in late cranial cartilage development Differentiation 2013 86 192 206 10.1016/j.diff.2013.07.006
Ewels P.A. Peltzer A. Fillinger S. Patel H. Alneberg J. Wilm A. Garcia M.U. Di Tommaso P. Nahnsen S. The nf-core framework for community-curated bioinformatics pipelines Nat. Biotechnol. 2020 38 276 278 10.1038/s41587-020-0439-x 32055031
Love M.I. Huber W. Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol. 2014 15 550 10.1186/s13059-014-0550-8
Kanehisa M. Sato Y. Kawashima M. KEGG mapping tools for uncovering hidden features in biological data Protein Sci. 2022 31 47 53 10.1002/pro.4172
Kanehisa M. Goto S. KEGG: Kyoto encyclopedia of genes and genomes Nucleic Acids Res. 2000 28 27 30 10.1093/nar/28.1.27 10592173
R Core Team R: A Language and Environment for Statistical Computing (4.0.2) R Foundation for Statistical Computing Vienna, Austria 2020 Available online: http://www.r-project.org/index.html (accessed on 9 March 2023)
Venables W.N. Ripley B.D. Modern Applied Statistics with S 4th ed. Springer New York, NY, USA 2002 0-387-95457-0
Pinheiro J. Bates D.M. Mixed-Effects Models in S and S-PLUS Springer New York, NY, USA 2000 10.1007/b98882
Fox J. Weisberg S. An {R} Companion to Applied Regression 3rd ed. SAGE Publications Inc. Thousand Oaks, CA, USA 2019 Available online: https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (accessed on 9 March 2023)
Lenth R.V. Emmeans: Estimated Marginal Means, aka Least-Squares Means R Package Version 1.7.5 R Foundation for Statistical Computing Vienna, Austria 2022 Available online: https://CRAN.R-project.org/package=emmeans (accessed on 9 March 2023)
Lenth R.V. Least-Squares Means: The R Package lsmeans J. Stat. Softw. 2016 69 1 33 10.18637/jss.v069.i01
Pelka K.E. Henn K. Keck A. Sapel B. Braunbeck T. Size does matter–Determination of the critical molecular size for the uptake of chemicals across the chorion of zebrafish (Danio rerio) embryos Aquat. Toxicol. 2017 185 1 10 10.1016/j.aquatox.2016.12.015 28142078
Khezri A. Fraser T.W. Nourizadeh-Lillabadi R. Kamstra J.H. Berg V. Zimmer K.E. Ropstad E. A Mixture of Persistent Organic Pollutants and Perfluorooctanesulfonic Acid Induces Similar Behavioural Responses, but Different Gene Expression Profiles in Zebrafish Larvae Int. J. Mol. Sci. 2017 18 291 10.3390/ijms18020291 28146072
Christou M. Fraser T.W.K. Berg V. Ropstad E. Kamstra J.H. Calcium signaling as a possible mechanism behind increased locomotor response in zebrafish larvae exposed to a human relevant persistent organic pollutant mixture or PFOS Environ. Res. 2020 187 109702 10.1016/j.envres.2020.109702
Fox K. Zauke G.P. Butte W. Kinetics of bioconcentration and clearance of 28 polychlorinated biphenyl congeners in zebrafish (Brachydanio rerio) Ecotoxicol. Env. Saf. 1994 28 99 109 10.1006/eesa.1994.1038 7523072
US-EPA Emerging Contaminants Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Emerging Contaminants Fact Sheet; Report 505F14001 2014 Available online: https://nepis.epa.gov (accessed on 8 April 2023)
De Silva A.O. Armitage J.M. Bruton T.A. Dassuncao C. Heiger-Bernays W. Hu X.C. Karrman A. Kelly B. Ng C. Robuck A. et al. PFAS Exposure Pathways for Humans and Wildlife: A Synthesis of Current Knowledge and Key Gaps in Understanding Environ. Toxicol. Chem. 2021 40 631 657 10.1002/etc.4935 33201517
Sunderland E.M. Hu X.C. Dassuncao C. Tokranov A.K. Wagner C.C. Allen J.G. A review of the pathways of human exposure to poly- and perfluoroalkyl substances (PFASs) and present understanding of health effects J. Expo. Sci. Environ. Epidemiol. 2019 29 131 147 10.1038/s41370-018-0094-1
Sinclair G.M. Long S.M. Jones O.A.H. What are the effects of PFAS exposure at environmentally relevant concentrations? Chemosphere 2020 258 127340 10.1016/j.chemosphere.2020.127340 32563917
Kato K. Ye X. Calafat A.M. PFASs in the General Population Toxicological Effects of Perfluoroalkyl and Polyfluoroalkyl Substances De Witt J.C. Series Molecular and Integrative Toxicology; Nunes, C., Ed. Humana Press Totowa, NJ, USA 2015 51 76 10.1007/978-3-319-15518-0
Wasel O. Thompson K.M. Freeman J.L. Assessment of unique behavioral, morphological, and molecular alterations in the comparative developmental toxicity profiles of PFOA, PFHxA, and PFBA using the zebrafish model system Environ. Int. 2022 170 107642 10.1016/j.envint.2022.107642
Jantzen C.E. Annunziato K.A. Bugel S.M. Cooper K.R. PFOS, PFNA, and PFOA sub-lethal exposure to embryonic zebrafish have different toxicity profiles in terms of morphometrics, behavior and gene expression Aquat. Toxicol. 2016 175 160 170 10.1016/j.aquatox.2016.03.026
Usenko C.Y. Robinson E.M. Usenko S. Brooks B.W. Bruce E.D. PBDE developmental effects on embryonic zebrafish Environ. Toxicol. Chem. 2011 30 1865 1872 10.1002/etc.570
Singleman C. Zimmerman A. Harrison E. Roy N.K. Wirgin I. Holtzman N.G. Toxic Effects of Polychlorinated Biphenyl Congeners and Aroclors on Embryonic Growth and Development Environ. Toxicol. Chem. 2021 40 187 201 10.1002/etc.4908
OECD Test No. 236: Fish Embryo Acute Toxicity (FET) Test OECD Publishing Paris, France 2013
Abe F.R. de Oliveira A.A.S. Marino R.V. Rialto T.C.R. Oliveira D.P. Dorta D.J. A comparison of developmental toxicity of brominated and halogen-free flame retardant on zebrafish Ecotoxicol. Environ. Saf. 2021 208 111745 10.1016/j.ecoenv.2020.111745
Godfrey A. Hooser B. Abdelmoneim A. Horzmann K.A. Freemanc J.L. Sepulveda M.S. Thyroid disrupting effects of halogenated and next generation chemicals on the swim bladder development of zebrafish Aquat. Toxicol. 2017 193 228 235 10.1016/j.aquatox.2017.10.024
Raldua D. Babin P.J. Simple, rapid zebrafish larva bioassay for assessing the potential of chemical pollutants and drugs to disrupt thyroid gland function Environ. Sci. Technol. 2009 43 6844 6850 10.1021/es9012454 19764258
Loosli F. Staub W. Finger-Baier K.C. Ober E.A. Verkade H. Wittbrodt J. Baier H. Loss of eyes in zebrafish caused by mutation of chokh/rx3 EMBO Rep. 2003 4 894 899 10.1038/sj.embor.embor919
Pavlou S. Astell K. Kasioulis I. Gakovic M. Baldock R. van Heyningen V. Coutinho P. Pleiotropic effects of Sox2 during the development of the zebrafish epithalamus PLoS ONE 2014 9 e87546 10.1371/journal.pone.0087546
Chassaing N. Sorrentino S. Davis E.E. Martin-Coignard D. Iacovelli A. Paznekas W. Webb B.D. Faye-Petersen O. Encha-Razavi F. Lequeux L. et al. OTX2 mutations contribute to the otocephaly-dysgnathia complex J. Med. Genet. 2012 49 373 379 10.1136/jmedgenet-2012-100892 22577225
Takamiya M. Stegmaier J. Kobitski A.Y. Schott B. Weger B.D. Margariti D. Cereceda Delgado A.R. Gourain V. Scherr T. Yang L. et al. Pax6 organizes the anterior eye segment by guiding two distinct neural crest waves PLoS Genet. 2020 16 e1008774 10.1371/journal.pgen.1008774 32555736
Li Z. Ptak D. Zhang L. Walls E.K. Zhong W. Leung Y.F. Phenylthiourea specifically reduces zebrafish eye size PLoS ONE 2012 7 e40132 10.1371/journal.pone.0040132
Kim K.T. Zaikova T. Hutchison J.E. Tanguay R.L. Gold nanoparticles disrupt zebrafish eye development and pigmentation Toxicol. Sci. 2013 133 275 288 10.1093/toxsci/kft081
Barbagallo S. Baldauf C. Orosco E. Roy N.M. Di-butyl phthalate (DBP) induces defects during embryonic eye development in zebrafish Ecotoxicology 2022 31 178 185 10.1007/s10646-021-02468-5
Wang Y.P. Hong Q. Qin D.N. Kou C.Z. Zhang C.M. Guo M. Guo X.R. Chi X. Tong M.L. Effects of embryonic exposure to polychlorinated biphenyls on zebrafish (Danio rerio) retinal development J. Appl. Toxicol. 2012 32 186 193 10.1002/jat.1650
Li M. Yang T. Gao L. Xu H. An inadvertent issue of human retina exposure to endocrine disrupting chemicals: A safety assessment Chemosphere 2021 264 128484 10.1016/j.chemosphere.2020.128484 33022499
Seipold S. Priller F.C. Goldsmith P. Harris W.A. Baier H. Abdelilah-Seyfried S. Non-SMC condensin I complex proteins control chromosome segregation and survival of proliferating cells in the zebrafish neural retina BMC Dev. Biol. 2009 9 40 10.1186/1471-213X-9-40 19586528
Hagenaars A. Vergauwen L. De Coen W. Knapen D. Structure-activity relationship assessment of four perfluorinated chemicals using a prolonged zebrafish early life stage test Chemosphere 2011 82 764 772 10.1016/j.chemosphere.2010.10.076
Gong H. Du J. Xu J. Yang Y. Lu H. Xiao H. Perfluorononanoate and Perfluorobutane Sulfonate Induce Cardiotoxic Effects in Zebrafish Environ. Toxicol. Chem. 2022 41 2527 2536 10.1002/etc.5447 35899994
Singleman C. Holtzman N.G. PCB and TCDD derived embryonic cardiac defects result from a novel AhR pathway Aquat. Toxicol. 2021 233 105794 10.1016/j.aquatox.2021.105794
Everett C.J. Mainous A.G. 3rd Frithsen I.L. Player M.S. Matheson E.M. Association of polychlorinated biphenyls with hypertension in the 1999-2002 National Health and Nutrition Examination Survey Environ. Res. 2008 108 94 97 10.1016/j.envres.2008.05.006 18606400
Wu M. Zuo Z. Li B. Huang L. Chen M. Wang C. Effects of low-level hexabromocyclododecane (HBCD) exposure on cardiac development in zebrafish embryos Ecotoxicology 2013 22 1200 1207 10.1007/s10646-013-1107-4
El-Nahhal Y. El-Nahhal I. Cardiotoxicity of some pesticides and their amelioration Environ. Sci. Pollut. Res. Int. 2021 28 44726 44754 10.1007/s11356-021-14999-9
Loerracher A.K. Braunbeck T. Cytochrome P450-dependent biotransformation capacities in embryonic, juvenile and adult stages of zebrafish (Danio rerio)-a state-of-the-art review Arch. Toxicol. 2021 95 2299 2334 10.1007/s00204-021-03071-7
Schmidt K. Steinberg C.E.W. Pflugmacher S. Staaks G.B.O. Xenobiotic substances such as PCB mixtures (Aroclor 1254) and TBT can influence swimming behavior and biotransformation activity (GST) of carp (Cyprinus carpio) Environ. Toxicol. 2004 19 460 470 10.1002/tox.20051
Schmidt K. Staaks G.B.O. Pflugmacher S. Steinberg C.E.W. Impact of PCB mixture (Aroclor 1254) and TBT and a mixture of both on swimming behavior, body growth and enzymatic biotransformation activities (GST) of young carp (Cyprinus carpio) Aquat. Toxicol. 2005 71 49 59 10.1016/j.aquatox.2004.10.012 15642631
Haimbaugh A. Wu C.C. Akemann C. Meyer D.N. Connell M. Abdi M. Khalaf A. Johnson D. Baker T.R. Multi- and Transgenerational Effects of Developmental Exposure to Environmental Levels of PFAS and PFAS Mixture in Zebrafish (Danio rerio) Toxics 2022 10 334 10.3390/toxics10060334 35736942
Fraser T.W.K. Khezri A. Lewandowska-Sabat A.M. Henry T. Ropstad E. Endocrine disruptors affect larval zebrafish behavior: Testing potential mechanisms and comparisons of behavioral sensitivity to alternative biomarkers Aquat. Toxicol. 2017 193 128 135 10.1016/j.aquatox.2017.10.002 29078070
Yaghoobi B. Miller G.W. Holland E.B. Li X. Harvey D. Li S. Lehmler H.J. Pessah I.N. Lein P.J. Ryanodine receptor-active non-dioxin-like polychlorinated biphenyls cause neurobehavioral deficits in larval zebrafish Front. Toxicol. 2022 4 947795 10.3389/ftox.2022.947795 36278027
Lee S. Ko E. Lee H. Kim K.T. Choi M. Shin S. Mixed Exposure of Persistent Organic Pollutants Alters Oxidative Stress Markers and Mitochondrial Function in the Tail of Zebrafish Depending on Sex Int. J. Environ. Res. Public Health 2021 18 9539 10.3390/ijerph18189539
Ko E. Kim D. Kim K. Choi M. Shin S. The action of low doses of persistent organic pollutants (POPs) on mitochondrial function in zebrafish eyes and comparison with hyperglycemia to identify a link between POPs and diabetes Toxicol. Mech. Methods 2020 30 275 283 10.1080/15376516.2020.1717704
Jochum W. Passegue E. Wagner E.F. AP-1 in mouse development and tumorigenesis Oncogene 2001 20 2401 2412 10.1038/sj.onc.1204389
Knuth M.M. Mahapatra D. Jima D. Wan D. Hammock B.D. Law M. Kullman S.W. Vitamin D deficiency serves as a precursor to stunted growth and central adiposity in zebrafish Sci. Rep. 2020 10 16032 10.1038/s41598-020-72622-2
Aceto J. Nourizadeh-Lillabadi R. Maree R. Dardenne N. Jeanray N. Wehenkel L. Alestrom P. van Loon J.J. Muller M. Zebrafish bone and general physiology are differently affected by hormones or changes in gravity PLoS ONE 2015 10 e0126928 10.1371/journal.pone.0126928
Su T. Ding X. Regulation of the cytochrome P450 2A genes Toxicol. Appl. Pharmacol. 2004 199 285 294 10.1016/j.taap.2003.11.029 15364544
Goldstone J.V. McArthur A.G. Kubota A. Zanette J. Parente T. Jonsson M.E. Nelson D.R. Stegeman J.J. Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish BMC Genom. 2010 11 643 10.1186/1471-2164-11-643 21087487
Kubota A. Bainy A.C. Woodin B.R. Goldstone J.V. Stegeman J.J. The cytochrome P450 2AA gene cluster in zebrafish (Danio rerio): Expression of CYP2AA1 and CYP2AA2 and response to phenobarbital-type inducers Toxicol. Appl. Pharm. 2013 272 172 179 10.1016/j.taap.2013.05.017 23726801
Hartig E.I. Zhu S. King B.L. Coffman J.A. Cortisol-treated zebrafish embryos develop into pro-inflammatory adults with aberrant immune gene regulation Biol. Open 2016 5 1134 1141 10.1242/bio.020065
Delcourt N. Quevedo C. Nonne C. Fons P. O’Brien D. Loyaux D. Diez M. Autelitano F. Guillemot J.C. Ferrara P. et al. Targeted identification of sialoglycoproteins in hypoxic endothelial cells and validation in zebrafish reveal roles for proteins in angiogenesis J. Biol. Chem. 2015 290 3405 3417 10.1074/jbc.M114.618611
Hao R. Bondesson M. Singh A.V. Riu A. McCollum C.W. Knudsen T.B. Gorelick D.A. Gustafsson J.A. Identification of estrogen target genes during zebrafish embryonic development through transcriptomic analysis PLoS ONE 2013 8 e79020 10.1371/journal.pone.0079020
Haggard D.E. Noyes P.D. Waters K.M. Tanguay R.L. Transcriptomic and phenotypic profiling in developing zebrafish exposed to thyroid hormone receptor agonists Reprod. Toxicol. 2018 77 80 93 10.1016/j.reprotox.2018.02.006
European Chemical Agency Per- and Polyfluoroalkyl Substances (PFASs) 2023 Available online: https://echa.europa.eu/hot-topics/perfluoroalkyl-chemicals-pfas (accessed on 3 March 2023)
US-EPA Per- and Polyfluoroalkyl Substances (PFAS) 2023 Available online: https://www.epa.gov/pfas (accessed on 6 March 2023)
Focus features. Dark Waters, YouTube 2019 Available online: https://www.youtube.com/watch?v=RvAOuhyunhY (accessed on 6 March 2023)
Rich N. The Lawyer Who Became DuPont’s Worst Nightmare The New York Times 2016 Available online: https://www.nytimes.com/2016/2001/2010/magazine/the-lawyer-who-became-duponts-worst-nightmare.html (accessed on 16 March 2023)
Salvidge R. Hosea L. What Are PFAS, How Toxic Are They and How Do You Become Exposed? Everything You Need to Know about ‘Forever Chemicals’ Detected in Air, Water, Soils, Sediments and Rain The Guardian 2023 Available online: https://www.theguardian.com/environment/2023/feb/2023/what-are-pfas-forever-chemicals-how-toxic-are-they-and-how-do-you-become-exposed (accessed on 16 March 2023)
Edgar R. Domrachev M. Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res. 2002 30 207 210 10.1093/nar/30.1.207